The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria
Abstract Translational control in pathogenic bacteria is fundamental to gene expression and affects virulence and other infection phenotypes. We used an enhanced ribosome profiling protocol coupled with parallel transcriptomics to capture accurately the global translatome of two evolutionarily dista...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-12-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-43759-1 |
| _version_ | 1797397892824039424 |
|---|---|
| author | Owain J. Bryant Filip Lastovka Jessica Powell Betty Y. -W. Chung |
| author_facet | Owain J. Bryant Filip Lastovka Jessica Powell Betty Y. -W. Chung |
| author_sort | Owain J. Bryant |
| collection | DOAJ |
| description | Abstract Translational control in pathogenic bacteria is fundamental to gene expression and affects virulence and other infection phenotypes. We used an enhanced ribosome profiling protocol coupled with parallel transcriptomics to capture accurately the global translatome of two evolutionarily distant pathogenic bacteria—the Gram-negative bacterium Salmonella and the Gram-positive bacterium Listeria. We find that the two bacteria use different mechanisms to translationally regulate protein synthesis. In Salmonella, in addition to the expected correlation between translational efficiency and cis-regulatory features such as Shine–Dalgarno (SD) strength and RNA secondary structure around the initiation codon, our data reveal an effect of the 2nd and 3rd codons, where the presence of tandem lysine codons (AAA-AAA) enhances translation in both Salmonella and E. coli. Strikingly, none of these features are seen in efficiently translated Listeria transcripts. Instead, approximately 20% of efficiently translated Listeria genes exhibit 70 S footprints seven nt upstream of the authentic start codon, suggesting that these genes may be subject to a novel translational initiation mechanism. Our results show that SD strength is not a direct hallmark of translational efficiency in all bacteria. Instead, Listeria has evolved additional mechanisms to control gene expression level that are distinct from those utilised by Salmonella and E. coli. |
| first_indexed | 2024-03-09T01:16:46Z |
| format | Article |
| id | doaj.art-a64572d58e3644139cce19a315547ebe |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-09T01:16:46Z |
| publishDate | 2023-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-a64572d58e3644139cce19a315547ebe2023-12-10T12:25:36ZengNature PortfolioNature Communications2041-17232023-12-0114111510.1038/s41467-023-43759-1The distinct translational landscapes of gram-negative Salmonella and gram-positive ListeriaOwain J. Bryant0Filip Lastovka1Jessica Powell2Betty Y. -W. Chung3Department of Pathology, University of CambridgeDepartment of Pathology, University of CambridgeDepartment of Pathology, University of CambridgeDepartment of Pathology, University of CambridgeAbstract Translational control in pathogenic bacteria is fundamental to gene expression and affects virulence and other infection phenotypes. We used an enhanced ribosome profiling protocol coupled with parallel transcriptomics to capture accurately the global translatome of two evolutionarily distant pathogenic bacteria—the Gram-negative bacterium Salmonella and the Gram-positive bacterium Listeria. We find that the two bacteria use different mechanisms to translationally regulate protein synthesis. In Salmonella, in addition to the expected correlation between translational efficiency and cis-regulatory features such as Shine–Dalgarno (SD) strength and RNA secondary structure around the initiation codon, our data reveal an effect of the 2nd and 3rd codons, where the presence of tandem lysine codons (AAA-AAA) enhances translation in both Salmonella and E. coli. Strikingly, none of these features are seen in efficiently translated Listeria transcripts. Instead, approximately 20% of efficiently translated Listeria genes exhibit 70 S footprints seven nt upstream of the authentic start codon, suggesting that these genes may be subject to a novel translational initiation mechanism. Our results show that SD strength is not a direct hallmark of translational efficiency in all bacteria. Instead, Listeria has evolved additional mechanisms to control gene expression level that are distinct from those utilised by Salmonella and E. coli.https://doi.org/10.1038/s41467-023-43759-1 |
| spellingShingle | Owain J. Bryant Filip Lastovka Jessica Powell Betty Y. -W. Chung The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria Nature Communications |
| title | The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria |
| title_full | The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria |
| title_fullStr | The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria |
| title_full_unstemmed | The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria |
| title_short | The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria |
| title_sort | distinct translational landscapes of gram negative salmonella and gram positive listeria |
| url | https://doi.org/10.1038/s41467-023-43759-1 |
| work_keys_str_mv | AT owainjbryant thedistincttranslationallandscapesofgramnegativesalmonellaandgrampositivelisteria AT filiplastovka thedistincttranslationallandscapesofgramnegativesalmonellaandgrampositivelisteria AT jessicapowell thedistincttranslationallandscapesofgramnegativesalmonellaandgrampositivelisteria AT bettyywchung thedistincttranslationallandscapesofgramnegativesalmonellaandgrampositivelisteria AT owainjbryant distincttranslationallandscapesofgramnegativesalmonellaandgrampositivelisteria AT filiplastovka distincttranslationallandscapesofgramnegativesalmonellaandgrampositivelisteria AT jessicapowell distincttranslationallandscapesofgramnegativesalmonellaandgrampositivelisteria AT bettyywchung distincttranslationallandscapesofgramnegativesalmonellaandgrampositivelisteria |